Skip to main content
Log in

A proposed neural network for the integrator of the oculomotor system

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Single-unit recordings, stimulation studies, and eye movement measurements all indicate that the firing patterns of many oculomotor neurons in the brain stem encode eye-velocity commands in premotor circuits while the firing patterns of extraocular motoneurons contain both eye-velocity and eye-position components. It is necessary to propose that the eye-position component is generated from the eye-velocity signal by a leaky hold element or temporal integrator. Prior models of this integrator suffer from two important problems. Since cells appear to have a steady, background signal when eye position and velocity are zero, how does the integrator avoid integrating this background rate? Most models employ some form of lumped, oositive feedback the gain of which must be kept within totally unreasonable limits for proper operation. We propose a lateral inhibitory network of homogeneous neurons as a model for the neural integrator that solves both problems. Parameter sensitivity studies and lesion simulations are presented to demonstrate robustness of the model with respect to both the choice of parameter values and the consequences of pathological changes in a portion of the neural integrator pool.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abel, L.A., Dell'Osso, L.F., Daroff, R.B.: Analog model for gazeevoked nystagmus. IEEE Trans. Biomed. Eng.25:1, 71–75 (1978)

    Google Scholar 

  • van der Heiden, U.: Analysis of neural networks. In: Lecture notes in biomathematics. Levin, S. (ed.), pp. 12–13. Berlin, Heidelberg, New York: Springer 1980

    Google Scholar 

  • Becker, W., Klein, H.: Accuracy of saccadic eye movements and maintenance of eccentric eye positions in the dark. Vision Res.13, 1021–1034 (1973)

    Google Scholar 

  • Cohen, B., Komatsuzaki, A.: Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. Exp. Neurol.36, 101–117 (1972)

    Google Scholar 

  • Doslak, M.J., Dell'Osso, L.F., Daroff, R.B.: A model of Alexander's law of vestibular nystagmus. Biol. Cybern.34, 181–186 (1979)

    Google Scholar 

  • Ermantrout, G.B., Cowan, J.D.: Large scale spatially organized activity in neural Nets. SIAM J. Applied Math.38, 1–21 (1980)

    Google Scholar 

  • Kamath, B.Y., Keller, E.L.: A neurological integrator for the oculomotor control system. Math. Biosci.30, 341–352 (1976)

    Google Scholar 

  • Keller, E.L.: Participation of medial pontine reticular formation in eye movement generation in monkey. J. Neurophysiol.37, 316–322 (1974)

    Google Scholar 

  • Nagel, L.W.: SPICE 2: a computer to simulate semiconductor circuits, ERL Memo No. ERL-M520, Electronics Research Laboratory, Univ. of Calif., Berkeley (1975)

    Google Scholar 

  • Optican, L.M., Robinson, D.A.: Cerebellar-dependent adaptive control of primate saccadic system. J. Neurophysiol.44, 1058–1076 (1980)

    Google Scholar 

  • Rall, W.: Membrane potential transients and membrane time constants of motoneurons. Exp. Neurol.2, 503–532 (1960)

    Google Scholar 

  • Ratliff, K., Hartline, F.: Studies on excitation and inhibition in the retina. The Rockefeller University Press 1974

  • Ratliff, K., Knight, W.B., Graham, W.: On tuning and amplification by lateral inhibition. Proc. Natl. Acad. Sci.62, 733–740 (1969)

    Google Scholar 

  • Robinson, D.A.: Eye movement control in primates. Science161, 1219–1224 (1968)

    Google Scholar 

  • Robinson, D.A.: Models of oculomotor neural organization. In: The control of eye movements, Bach-y-Rita, P., Collins, C.C., Hyde, J.E. (eds.), pp. 519–538. New York: Academic Press 1971

    Google Scholar 

  • Robinson, D.A.: The effect of cerebellectomy on the cat's vestibuloocular integrator. Brain Res.71, 195–207 (1974)

    Google Scholar 

  • Robinson, D.A.: Oculomotor control signals. In: Basic mechanisms of ocular motility and their clinical implications. Bach-y-Rita, P., Lennerstrand, G. (eds.), pp. 337–374. Oxford: Pergamon Press 1975 (Wenner-Gren Cent. Int. Symp. Ser.)

    Google Scholar 

  • Rosen, M.J.: A theoretical neural integrator. IEEE Trans. Biomed. Eng.19, 362–367 (1972)

    Google Scholar 

  • Skavenski, A.A., Robinson, D.A.: Role of abducens neurons in vestibuloocular reflex. J. Neurophysiol.36, 724–738 (1973)

    Google Scholar 

  • van Gisbergen, J.A.M., Robinson, D.A., Gielen, S.: A quantitative analysis of the generation of saccadic eye movements by burst neurons. J. Neurophysiol.45, 417–442 (1981)

    Google Scholar 

  • Waespe, W., Henn, V.: Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp. Brain Res.27, 523–538 (1977)

    Google Scholar 

  • Zee, D.S., Friendlich, A.R., Robinson, D.A.: The mechanism of downbeat nystagmus. Arch. Neurol.30, 227–237 (1974)

    Google Scholar 

  • Zee, D.S., Yamazaki, A., Butler, P., Gucer, G.: Effect of ablation of flocculus and paraflocclus on eye movement in primate. J. Neurophysiol.46, 878–899 (1981)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cannon, S.C., Robinson, D.A. & Shamma, S. A proposed neural network for the integrator of the oculomotor system. Biol. Cybernetics 49, 127–136 (1983). https://doi.org/10.1007/BF00320393

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00320393

Keywords

Navigation